Lankesteriana ISSN: 1409-3871 Lankester Botanical Garden, University of Costa Rica

Besi, Edward E.; Nikong, Dome; Mustafa, Muskhazli; Go, Rusea Orchid diversity in anthropogenic-induced degraded tropical , an extrapolation towards conservation Lankesteriana, vol. 19, no. 2, 2019, May-August, pp. 107-124 Lankester Botanical Garden, University of Costa Rica

DOI: https://doi.org/10.15517/lank.v19i2.38775

Available in: https://www.redalyc.org/articulo.oa?id=44366684005

How to cite Complete issue Scientific Information System Redalyc More information about this article Network of Scientific Journals from Latin America and the Caribbean, Spain and Journal's webpage in redalyc.org Portugal Project academic non-profit, developed under the open access initiative LANKESTERIANA 19(2): 107–124. 2019. doi: http://dx.doi.org/10.15517/lank.v19i2.38775

ORCHID DIVERSITY IN ANTHROPOGENIC-INDUCED DEGRADED TROPICAL RAINFOREST, AN EXTRAPOLATION TOWARDS CONSERVATION

Edward E. Besi, Dome Nikong, Muskhazli Mustafa & Rusea Go*

Department of Biology, Faculty of Science, Universiti Putra , 43400 Serdang, Selangor Darul Ehsan, Malaysia *Corresponding author: [email protected]

Abstract. The uncontrolled logging in Peninsular Malaysia and the resulting mudslides in the lowland areas have been perilous, not to just humans, but also to another biodiversity, including the wild orchids. Their survival in these highly depleted areas is being overlooked due to the inaccessible and harsh environment. This paper reports on the rescue of orchids at risk from the disturbed forests for ex-situ conservation, the identification of the diversity of orchids and the evaluation of the influence of micro-climatic changes induced by clear-cut logging towards the resilience of orchids in the flood-disturbed secondary forests and logged forests in Terengganu and , located at the central region of Peninsular Malaysia, where the forest destruction by logging activities has been extensive. 109 orchid belonging to 40 genera were collected from the disturbed areas. The diversity and data analyses show that the disturbed secondary forests had a higher orchid density (0.0133 / m2) than the logged sites (0.0040 plants/m2) as the habitat conditions were more dependable. Nevertheless, the logged forests harboured a higher diversity of orchids (H=4.50 and D=0.99) of which 97.9% were . Eleven rare species were found along with six species endemic to Peninsular Malaysia, with two species new to science. The results highlighted the factors that allow the orchids to flourish or suffer in the disturbed forests. The logged forests had a higher ambient temperature and lower moisture level than the mud flood-disturbed and canopy-covered secondary forests. Apart from the extensive ground vegetation due to logs dragging extraction, low soil moisture and absence of leaf litter were believed to be the major attributes causing the low abundance of terrestrial orchids. The high abundance and diversity of epiphytic orchids and the large difference of their densities between the logged sites were influenced by the densities of fallen trees hosting orchid(s), disturbance- induced dryness stresses, durations of exposure to the anthropogenic-induced disturbance, and less favourable soil conditions for the terrestrial orchids. Key words: conservation, diversity, dryness stress, ecology, , logged forest, mudslides,

Introduction. Kuala Koh, Kelantan and Tasek Kenyir, and Bateq (Kuala Koh, Kelantan). The tribal people Terengganu are the largest and commonly visited parts forage the forest for food and medicines apart from of the Peninsular Malaysia’s National Park. Both are hunting and fishing for their daily necessities (Ramle located in the northeast states of Peninsular Malaysia. 1993, Fatanah 2009, Ramle et al. 2014, Abdullah et Tasek Kenyir is an artificial lake formed by Kenyir al. 2017). Topographically, the Kuala Koh and its Dam or the Sultan Mahmud Hydro-Electric Power adjacent area consist of riverine, largely hill and Station, which took 15 years to be constructed and fully lowland dipterocarp forests. The shaded and humid operate in 1978. Both areas are gazetted as a protected environment encourages the growth of mosses on forest reserve under the Taman Negara (Kelantan) the trees, creating niches suitable for moisture-loving Enactment [En. 14 of 1938] and the Taman Negara epiphytes. In over logged forest, epiphytic orchids are (Terengganu) Enactment [En. 6 of 1939]. These Acts also found growing in abundance on the ground and on are independent from The National Parks Act 1980. rocks, and a few relying on dead debris living as myco- These areas have many geological and biological heterotrophs. However, both terrestrial and epiphytic attractions (Hairul et al. 2016), apart from being home orchids have experienced population declined mainly for the aboriginal tribes of Semaq (Hulu Terengganu) because of habitat degradation and timber extraction

Received 27 March 2019; accepted for publication 06 August 2019. First published online: 27 August 2019. Licensed under a Creative Commons Attribution-NonCommercial-No Derivs 3.0 Costa Rica License. 108 LANKESTERIANA process, which have caused many species to near topsoil and nutrient were detrimental for the orchid extinction (Larson 1992, Rauh 1992, Dimmitt 2000, survival (Wan Mohd Shukri et al. 2007). Coupled with Mondragon & Calvo-Irabien 2006). rampant forests destruction in the surrounding areas, the The Orchidaceae is a speciose of mudslides have also negatively affected the ecosystem considerable significance in horticulture (Hew et al. balance, especially for the forest floor biodiversity 1997), and traditional medicine, with many species in including terrestrial orchids and waterways. various genera having been reported to have therapeutic Deforestation and the global climate change have properties (Pant 2013). Unfortunately, many orchids are been largely ignored by the authority due to lack of naturally rare, endangered, or vulnerable, for climate assessing personnel willing to work in dangerous fragile and habitat changes that are often anthropogenic, and logging sites, thus a stumbling block for conservation from over-collection for horticulture and medicine. efforts to protect forest biodiversity including orchids Some 972 species of orchids in 159 genera have in Malaysia. Because of their ecological, economical been recorded in Peninsular Malaysia (Go & Hamzah and pharmaceutical importance, an exhaustive 2008, Go et al. 2010, Kiew et al. 2010, Ong et al. evaluation on the diversity and ecology of orchids 2017). About twenty percent of them are endemic to in the degraded forest areas is crucial for setting its Peninsular Malaysia (Seidenfaden & Wood 1992, conservation priorities. Hence, this paper focuses on Turner 1995, Ong et al. 2011). Until recently, a total reporting the diversity and distribution of orchids at risk of 245 orchid species were collected from Terengganu in the degraded forests by uncovering the significance and 223 orchid species from Kelantan as documented of ecological alterations that are negatively affecting in SING (2018, January), Swiss Orchid their survival and to provide inference for ex-situ Foundation at the Herbarium Jany Renz (2017, July), conservation plans. National Herbarium of the Netherlands (NHN) (2017, July), Turner (1995), and Jaafar et al. (2007). Materials and Methods In recent years, human activities in Kuala Koh Selection of field sampling localities and ecosystems.– and around Tasek Kenyir have directly threatened the The study areas were classified based on the type survivability of biodiversity including orchids. Kuala of disturbance: disturbed secondary forests (DSFs) Koh and its vicinities are now blatantly known to have damaged by mudslides, and logging sites. Observations the highest rate of deforestation in Peninsular Malaysia. and botanical collection trips were carried out in the A large tract of forest near the National Park entrance disturbed forests of Terengganu and Kelantan regions has been cleared for farming, mining and logging from November 2016 until May 2018 (Fig. 1). The (Tuck-Po 2000, Lye 2005, Hairul et al. 2016). Forest areas covered in this study were DSFs in Kuala Koh, clearance has spread extensively to Tasek Kenyir Gua Musang, Kelantan (94.4–129.9 m a.s.l.) and area. The clay exposed cleared land caused surface Air Canal, Tanah Merah, Kelantan (44 m a.s.l.); and water run-off and land erosion due to lack of retention logging sites in Tasek Kenyir, Terengganu (98.8–330.4 from grasses, trees, and shrubs had caused the 2014 m a.s.l.). The disturbed forests were selected based tragic flash floods and mudslides in the lowland areas on whether logging was imminent, currently actively of Terengganu and Kelantan. Based on our empirical logged, and the recent deadly mudslides repercussion. observations, the uncontrolled and unsustainable Eight short line-transect plots of 20 m × 5 m with a timber production might have concurrently shoved the total area of 800 m2 were established in Kuala Koh. epiphytic orchid flora towards local extinction. The Meanwhile, two line-transect plots of 25 m × 5 m were canopy disruptions caused by timber extractions have created in disturbed lowland secondary forest at Air greatly modified the temperature, humidity, and light Canal with the total area of 250 m2. Three logging sites conditions, causing unfavourable habitat for the shade- in the Tasek Kenyir area were selected as study sites. loving species (Gradstein 2008, Benίtez et al. 2015). These sites were located using Google Maps and also Thus, the extremely harsh conditions in the logging based on an earlier preliminary empirical study. Site 1 sites (logged forests) where full exposure to the sun, and Site 2 of active logging were located in Gawi, and water stress, and nutrient-poor soil due to the eroded Site 3 was located in Petuang, with a total area studied

LANKESTERIANA 19(2). 2019. © Universidad de Costa Rica, 2019. Besi et al. — Orchid diversity in anthropogenic-induced degraded tropical rainforest 109

Figure 1. Coordinates of each studied site recorded in disturbed forests of Terengganu and Kelantan regions. A. Kuala Koh area (DSFs Site 1). B. Gawi area (Logging Site 1). C. Gawi area (Logging Site 2). D. Petuang area (Logging Site 3). E. Tanah Merah area (DSFs Site 2). The map was adapted from http://www.geoplaner.com, a free web-based application that provides several GIS and GPS services. of approximately 53,000 m2. The total area studied in standard herbarium technique after Bridson and Forman the logging sites was calculated based on the distance (2000) and the non-flowering ones were transplanted traveled along the logging road in the logging site into the ex-situ nursery, as living collections, where times the width of 20 m on each side of the road, and they were nurtured until flowering usually within five the orchids were mostly found on fallen trees. to six months, depending on the species (Go et al. 2011). Reliable references and online databases were Fieldwork and sample collection.– The systematic used in the identification process and evaluation of sampling involved choosing exploration sites based on each species’ distribution status: Seidenfaden & Wood the existence of disturbed forests in the Terengganu and (1992), Turner (1995), Comber (2001), Ong et al. Kelantan. The date and time of the sample collections (2017), the Swiss Orchid Foundation at the Herbarium were scheduled based on the type of disturbance Jany Renz. (2017, July), the National Herbarium of the (DSFs and logging site) and the accessibility (weighed Netherlands (NHN) accessed through Browse Dutch more towards the accessing highly disturbed and Natural History Collections: BioPortal (Naturalis) risky logging site areas). Non-flowering orchids were (2017, July), and the World Checklist of Selected transferred to an ex-situ facility in Setiu, Terengganu Families (WCSP) (2018, December). Also, expert for further flowering monitoring to ascertain the consultations were sought to make identifications. species identity. Diversity analyses.– Shannon-Wiener Diversity Index Sample processing and identification.– Identifiable (H) and Simpson’s Diversity Index (D) were used to samples (with floral structures) were preserved using determine the species richness and evenness in both

LANKESTERIANA 19(2). 2019. © Universidad de Costa Rica, 2019. 110 LANKESTERIANA studied areas. The Shannon index in real ecosystems ecological parameters between the different studied ranges between 1.5 and 3.5 (MacDonald 2003). The H sites with distinctively different disturbance types. The value rarely surpasses 4.5, and if it does increase, the significant difference of mean between groups was increment is small due to the logarithmic element in determined by comparing directly between the min the function (Margalef 1972). The greater the value, values recorded for DSFs with min values recorded for the higher the diversity. The D value ranges between logging sites and were also evaluated accordingly for 0 and 1; 1 represents infinite diversity and 0, no the max values. The Pearson’s correlation coefficient diversity. The closer the value is to 1, the higher the was used to measure the linear relationship between the diversity. However, these methods could not tell which orchid abundance and their host trees; Density of the factors contributed more to the value, hence, Evenness orchid species within a plot (plants/m2) and Density of (E) was used to determine how close in numbers each fallen trees hosting orchid(s) within a plot (plants/m2). species in each studied site (Help 1974). The E value is constrained between 0 and 1. The lower E value Results means the less evenness in the communities between Abundance and distribution pattern.– 132 orchid the species with presence of dominant species, and the specimens of 109 orchid species belonging to 40 lower the diversity. The formula is derived according to genera were collected from the disturbed forests (Table Pielou’s evenness index (Pielou 1966). The frequency 1). Of these, 116 orchid specimens belonging to 96 of occurrence of each species was determined based on species were recorded from the Tasek Kenyir logging the number of times that particular species occurs or sites, whereas, 16 specimens of 14 species were sighted at a specified sample plot. recorded from the DSFs. 93.3% of the total number of orchid species collected were epiphytes and 3.7% In-situ measurement of ecological data.– Minimum were terrestrials. Based on Table 1, orchid species (min) and maximum (max) values for four ecological collected from the disturbed forests were largely parameters were recorded from morning (10:00 a.m.) subfamily with 107 species (98.2%), to afternoon (4:00 p.m.) time in the studied disturbed and only one species was from Orchidoideae (0.9%) forests of Terengganu and Kelantan: temperature (ºC), and Apostasioideae (0.9%) subfamilies. Species of air relative humidity (ARH) (1–100%), soil moisture the genera Thouars and (SM) (1–10%), and light intensity (Lux or lx). Sw. were found to be the most abundant orchids living in these disturbed forests. The most abundant Data analyses.– All the data were recorded in a species found in the logging sites were Dendrobium spreadsheet, and the following parameters were crumenatum Sw. (3.2%) and Grammatophyllum computed as follows: 1) Density of the orchid species speciosum Blume (2.5%), whereas within a plot (plants/m2): Number of orchid species veratrifolia (Reinw.) Blume (3.2%) was abundant in within the plot (plants) / Total area of the plot (m2); the DSFs. A total of 87 species (79.8%) found in the 2) Density of fallen trees hosting orchid(s) within disturbed forests were growing with a sympodial habit. a plot (plants/m2): Number of fallen trees in the plot The remaining 22 species (20.2%) were monopodial, hosting orchids (plants) / Total area of the plot (m2); of which, 12 species (11%) were climbers. and 3) Relative abundance of orchid (%Ao): [Number of clump or population of a particular orchid species Rareness and endemism.– Ninety-two orchid species within the plot / Total number of all orchid clumps or (84.4%) collected were common and widespread. populations of the plot] × 100. Eleven orchid species (10.1%) were rare (recorded with a very narrow endemic range or less than Statistical analyses.– The ecological data were five locations of occupancy) or uncommon (more analysed using IBM SPSS version 19. Non-parametric abundant than a rare species) which were previously Kruskal-Wallis one-way analysis of variance (ANOVA) recorded with small distribution area. Six orchid with multiple pairwise comparisons (p<0.05) was species (5.5%) endemic to Peninsular Malaysia were used to determine the significant relationship of the also discovered; namely, Bulbophyllum linearifolium

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Table 1. List of orchid species collected from the disturbed forests of Terengganu and Kelantan, and details on their habit, abundance and distribution status. Notes: %Ao: Relative abundance of orchid; EP: Epiphyte; TR: Terrestrial; CM: Common; RR: Rare; NS: New Species; ED(PM): Endemic to Peninsular Malaysia. Growth Distribution Subfamily/ Species %Ao Habit Status Epidendroideae

Acriopsis 1. liliifolia (J.Koenig) Seidenf. var. liliifolia 1.3 EP CM

Adenoncos 2. Adenoncos major Ridl. 0.6 EP CM

3. Adenoncos vesiculosa Carr 0.6 EP CM

Aerides 4. odorata Lour. 1.3 EP CM

Agrostophyllum 5. glumaceum Hook.f. 0.6 EP CM

6. Agrostophyllum stipulatum subsp. bicuspidatum (J.J.Sm.) Schuit. 0.6 EP CM

7. Agrostophyllum stipulatum (Griff.) Schltr. subsp. stipulatum 0.6 EP CM

Appendicula 8. Appendicula lucida Ridl. 0.6 EP CM

9. Appendicula uncata Ridl. subsp. uncata 0.6 EP ED(PM)

Bromheadia 10. Bromheadia alticola Ridl. 0.6 EP CM

11. Bromheadia petuangensis Rusea & Besi sp. nov. 0.6 EP NS

Bulbophyllum 12. Bulbophyllum armeniacum J.J.Sm. 0.6 EP CM

13. Bulbophyllum bakhuizenii Steenis 0.6 EP CM

14. Bulbophyllum biflorum Teijsm. & Binn. 0.6 EP CM

15. Bulbophyllum biseriale Carr 0.6 EP CM

16. Bulbophyllum cf. caudatisepalum 0.6 EP CM

17. Bulbophyllum cf. corolliferum 0.6 EP CM

18. Bulbophyllum cf. flavescens 0.6 EP CM

19. Bulbophyllum corolliferum J.J.Sm. 1.9 EP CM

20. Bulbophyllum ecornutum (J.J.Sm.) J.J.Sm. subsp. ecornutum 0.6 EP RR

21. Bulbophyllum elevatopunctatum J.J.Sm. 0.6 EP RR

22. Bulbophyllum gracillimum (Rolfe) Rolfe 0.6 EP CM

23. Bulbophyllum lasiochilum E.C.Parish & Rchb.f. 0.6 EP RR

24. Bulbophyllum limbatum Lindl. 1.3 EP RR

25. Bulbophyllum linearifolium King & Pantl. 0.6 EP ED(PM)

26. Bulbophyllum macranthum Lindl. 0.6 EP CM

27. Bulbophyllum medusae (Lindl.) Rchb.f. 0.6 EP CM

28. Bulbophyllum patens King ex Hook.f. 0.6 EP CM

29. Bulbophyllum setuliferum J.J.Verm. & Saw 0.6 EP ED(PM)

30. Bulbophyllum sp. (1) 0.6 EP CM

31. Bulbophyllum vaginatum (Lindl.) Rchb.f. 1.3 EP CM 32. Bulbophyllum vermiculare Hook.f. 0.6 EP CM Calanthe 33. Calanthe ceciliae Rchb.f. 0.6 TR CM Callostylis 34. Callostylis pulchella (Lindl.) S.C.Chen & Z.H.Tsi 0.6 EP CM

Campanulorchis 35. Campanulorchis leiophylla (Lindl.) Y.P.Ng & P.J.Cribb 0.6 EP CM

36. Campanulorchis pellipes (Rchb.f. ex Hook.f.) Y.P.Ng & P.J.Cribb 1.3 EP CM

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Ceratostylis 37. Ceratostylis pendula Hook.f. 1.3 EP CM

38. Ceratostylis subulata Blume 0.6 EP CM

Cleisostoma 39. Cleisostoma discolor Lindl. 0.6 EP CM

40. Cleisostoma scortechinii (Hook.f.) Garay 0.6 EP CM

41. Cleisostoma sp. (1) 0.6 EP CM

Coelogyne 42. cumingii Lindl. 0.6 EP CM

43. Coelogyne foerstermannii Rchb.f. 1.3 EP CM

44. Coelogyne tomentosa Lindl. 0.6 EP CM

Corymborkis 45. Corymborkis veratrifolia (Reinw.) Blume 3.2 TR CM

Cylindrolobus 46. Cylindrolobus mucronatus (Lindl.) Rauschert 0.6 EP CM

47. Cylindrolobus neglectus (Ridl.) J.J.Wood 0.6 EP CM

Cymbidium 48. Cymbidium bicolor subsp. pubescens (Lindl.) Du Puy & P.J.Cribb 0.6 EP CM

49. Cymbidium finlaysonianum Lindl. 0.6 EP CM

Dendrobium 50. Dendrobium acerosum Lindl. 1.3 EP CM

51. Dendrobium angustifolium (Blume) Lindl. 0.6 EP CM

52. Dendrobium bancanum J.J.Sm. 1.9 EP CM

53. Dendrobium cf. linguella 0.6 EP CM

54. Dendrobium connatum (Blume) Lindl. var. connatum 0.6 EP CM

55. Dendrobium convexum (Blume) Lindl. 1.9 EP CM

56. Dendrobium crumenatum Sw. 3.2 EP CM

57. Dendrobium farmeri Paxton 0.6 EP CM

58. Dendrobium indivisum (Blume) Miq. var. indivisum 1.3 EP CM

59. Dendrobium indragiriense Schltr. 0.6 EP CM

60. Dendrobium kentrophyllum Hook.f. 0.6 EP CM

61. Dendrobium lamellatum (Blume) Lindl. 0.6 EP RR

62. Dendrobium leonis (Lindl.) Rchb.f. 1.3 EP CM

63. Dendrobium pachyphyllum (Kuntze) Bakh.f. 1.3 EP CM

64. Dendrobium plicatile Lindl. 0.6 EP CM

65. Dendrobium quadrilobatum Carr 1.3 EP RR

66. Dendrobium rhodostele Ridl. 0.6 EP CM

67. Dendrobium singaporense A.D.Hawkes & A.H.Heller 1.3 EP CM

68. Dendrobium sp. (1) 0.6 EP RR

69. Dendrobium tortile Lindl. 0.6 EP CM

70. Dendrobium zebrinum J.J.Sm. 0.6 EP CM

Dendrochilum 71. Dendrochilum pallidiflavens Blume var. pallidiflavens 0.6 EP CM

Eria 72. atrovinosa Carr 1.3 EP CM

73. Eria javanica (Sw.) Blume 0.6 EP CM

Grammatophyllum 74. Grammatophyllum speciosum Blume 2.5 EP CM

Grosourdya 75. Grosourdya cf. muscosa 0.6 EP RR

Liparis 76. Liparis elegans Lindl. 0.6 EP CM

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Micropera 77. Micropera fuscolutea (Lindl.) Garay 0.6 EP RR

78. Micropera pallida (Roxb.) Lindl. 0.6 EP CM

Mycaranthes 79. Mycaranthes latifolia Blume 0.6 EP CM

80. Mycaranthes pannea (Lindl.) S.C.Chen & J.J.Wood 1.3 EP CM

Oberonia 81. Oberonia brachystachys Lindl. 0.6 EP CM

82. Oberonia ciliolata Hook.f. 0.6 EP CM

83. Oberonia insectifera Hook.f. 0.6 EP CM

Oxystophyllum 84. Oxystophyllum carnosum Blume 1.9 EP CM

Pholidota 85. Pholidota articulata Lindl. 0.6 EP CM

Phreatia 86. plantaginifolia (J.Koenig) Ormerod 0.6 EP CM

Pinalia 87. Pinalia domii Rusea & Besi sp. nov. 0.6 EP NS

88. Pinalia floribunda (Lindl.) Kuntze 1.9 EP CM

89. Pinalia maingayi (Hook.f.) Kuntze 0.6 EP ED(PM)

Pomatocalpa 90. Pomatocalpa diffusum Breda 2.5 EP CM

91. Pomatocalpa spicatum Breda, Kuhl & Hasselt 1.9 EP CM

Renanthera 92. Renanthera histrionica Rchb.f. 0.6 EP CM

Rhynchostylis 93. Rhynchostylis retusa (L.) Blume 1.9 EP CM

Stichorkis 94. Stichorkis gibbosa (Finet) J.J.Wood 1.3 EP CM

Taeniophyllum 95. Taeniophyllum pusillum (Willd.) Seidenf. & Ormerod 0.6 EP RR

96. Taeniophyllum sp. (1) 0.6 EP RR

Thecostele 97. Thecostele alata (Roxb.) E.C.Parish & Rchb.f. 0.6 EP CM

Thelasis 98. carinata Blume 1.3 EP CM

99. Thelasis pygmaea (Griff.) Lindl. 0.6 EP CM 100. acuminatissimum (Blume) Rchb.f. subsp. Thrixspermum 1.3 EP CM acuminatissimum 101. Thrixspermum centipeda Lour. 1.3 EP CM

102. Thrixspermum cf. carnosum 0.6 EP CM

103. Thrixspermum clavatum (J.Koenig) Garay 0.6 EP CM

104. Thrixspermum sp. (1) 0.6 EP CM

105. Thrixspermum sp. (2) 0.6 EP CM

106. Thrixspermum trichoglottis (Hook.f.) Kuntze 0.6 EP CM

Trichotosia 107. Trichotosia gracilis (Hook.f.) Kraenzl. 0.6 EP CM

Apostasioideae

Apostasia 108. Apostasia nuda R.Br. 1.9 TR CM

Orchidoideae

Hetaeria 109. Hetaeria oblongifolia Blume 0.6 TR CM

King & Pantl., B. setuliferum J.J.Verm. & Saw, in Pakistan Journal of Botany) and Pinalia domii Pinalia maingayi (Hook.f.) Kuntze, Appendicula Rusea & Besi (unpublished). These new, rare, and uncata subsp. uncata Ridl. and including two species endemic species were all collected and rescued from new to science, which have been recently described: the logging sites. The logged forests were expected to Bromheadia petuangensis Rusea & Besi (in press have a higher likelihood harbouring rare and endemic

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Table 2. Comparison based on diversity and density of orchid species in DSFs of Kuala Koh, Gua Musang, Kelantan and Air Canal, Tanah Merah, Kelantan; and logging sites in Tasek Kenyir, Hulu Terengganu.

Studied sites Species richness Shannon Index, H Simpson Index, D Evenness, E Density (plants/m2)

DSFs 14 2.47 0.90 0.94 0.0133

Logging Sites 96 4.50 0.99 0.99 0.0040

Table 3. Diversity of epiphytic orchids found in the logging sites of Tasek Kenyir area.

Species Studied sites Shannon Index, H Simpson Index, D Evenness, E Density (plants/m2) richness Logging Sites 94 4.46 0.99 0.98 0.0013 species than the secondary forests, seeing that the Table 4. Comparison on densities of epiphytic orchid area covered was larger and the fallen trees provided species and fallen tree hosting orchid(s) between the the chance to harvest more epiphytic orchids which three studied logging sites in Tasek Kenyir area. are usually unreachable and difficult to see in the Gawi Gawi Petuang non-logged forests. Parameters (Site 1) (Site 2) (Site 3)

Diversity analyses and density.– Table 2 shows that Species Richness 26 33 51 the DSFs had a higher orchid density (0.0133 plants/ m2) when compared with the logging sites (0.0040 Number of Fallen Trees 2 Hosting Orchid(s) 19 29 25 plants/m ) although the total of the area covered (1,050 (plants) m2) was very much lower than the latter (73,550 m2). However, the logged forests had a higher diversity of Total Area Studied (m2) 10,000 9,500 53,000 orchid species (H=4.50 and D=0.99) compared with Density of Orchids the secondary forests (H=2.47 and D=0.90) with 94 0.0026 0.0035 0.0010 Species (plants/m2) species (97.9%) of the orchids encountered being epiphytes. The high H and D values are also supported Density of Fallen Trees 0.0019 0.0031 0.0005 by the high E values (E value of logging sites = 0.99 > Hosting Orchid(s) 2 E values of DSFs = 0.94) implies that the abundance (plants/m ) of clumps or populations of each species in the logging sites was evenly distributed without being dominated < Gawi (Site 1) = 10,000 m2 < Petuang (Site 3) = 53,000 by only one species. m2]. The densities of fallen trees hosting orchid(s) also The logging sites were dominated by epiphytic demonstrates a similar pattern; Gawi (Site 2) had a orchids which were found attached to the fallen trees higher density than the other studied sites [Gawi (Site within a 73,550 m2 area with a total density of 0.0013 2) = 0.0031 plants/m2 > Gawi (Site 1) = 0.0019 plants/ plants/m2 (Table 3). The H (H=4.46) and D (D=0.99) m2 > Petuang (Site 3) = 0.0005 plants/m2]. values were high indicating a high diversity of epiphytic Pearson’s correlation was performed to determine orchids (Table 3). The high E value (E=0.98), shows the correlation between the density of orchid species that the epiphytic orchid diversity was also influenced and density of fallen trees hosting orchid(s) in the by their evenly distributed abundance and absence of logging sites. Table 5 shows a significant and strong dominant species (Table 3). In comparison, according positive correlation between the densities of orchid to the data shown in Table 4 the density of epiphytic species and the densities of fallen trees hosting orchids in Gawi (Site 2) was higher [Gawi (Site 2) = orchid(s), r=0.993, n=3, p=0.037. This implies that a 0.0035 plants/m2 > Gawi (Site 1) = 0.0026 plants/m2 > single logging activity in a small area could accumulate Petuang (Site 3) = 0.0010 plants/m2] even though the and expose a high abundance and diversity of orchids total area studied was lower [Gawi (Site 2) = 9,500 m2 to imminent danger.

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Microclimate of the disturbed forests.– Table 6 of extreme low and high light intensities are 0–1,350 and Figure 2 show the significant difference of the lx and 17,550–24,300 lx, respectively (the values microclimate between DSFs and logging sites. recorded were converted from µmol m-2s-1 to Lux unit). The max temperature recorded in the clear logged The range normally used in a field study is between forests (34.9±1.0 ºC) was significantly higher 15,120–20,520 lx (Chen & Wang 1996). Based on the [H(1)=6.621, p=0.010] than in the DSFs with trees data collected on light intensities that also defines level canopies (31.1±0.3 ºC) (Figure 2B), with mean rank of illuminance, it does not inflict any injurious effects of 13.2 for logging sites and 5.5 for DSFs. The high as the values were still within the adaptable range. temperature recorded in logging sites was also linked However, the values recorded shown a slight deviation to its significantly lower min values [H(1)=5.889, from the specified range values of the used Lux meter, p=0.015] of ARH, with mean rank of 8.93 for logging where the standardized specification of the meter sites and 16.17 for DSFs (Figure 2C). Moreover, signifies the average outdoor sunlight normally ranged the microclimate values on temperature for both between 20,000 lx to 50,000 lx. The values recorded different types of disturbed forests are also much for logging sites only reached up to the max value of higher than the local climate’s; with mean value of 20,000 lx, in which, the light intensity for the opened Min Temperature = 23.2 ºC and mean value of Max canopies forest should have been at least 20,000 lx. Temperature = 30.9 ºC (Malaysian Meteorology Table 5. Correlation between number of epiphytic orchid Department 2016, 2017). Simultaneously, both areas species and the number of fallen trees hosting orchid(s) would have had lower ARH if compared to the local found in the logging sites of Tasek Kenyir area. climate with mean value of ARH is 86.8% (Malaysian *Correlation is significant at the 0.05 level (1-tailed). Meteorology Department 2016, 2017). This could imply that the microclimate of disturbed forests was Pearson’s Correlation Coefficient much more intense if compared to the local climate of Density of Orchid the surrounding areas. Species The SM level shows a similar pattern where the Pearson Correlation 1 min and max values of SM recorded for logging sites Density of Orchid were lower than DSFs, although the difference was Species not statistically significant due to the small sample Sig. (1-tailed) size studied and limited accessible area in the DSFs N 3 Pearson (Figure 2G–H). 0.993* Correlation Optimum range of light intensities on orchid Density of Fallen Trees development was referred to Guo et al. (2012), a Hosting Orchid(s) Sig. (1-tailed) 0.037 study tested on wild , where the range N 3

Table 6. Summary of topographic and ecological predictors (mean±SE) of DSFs in Kuala Koh, Gua Musang, Kelantan and Air Canal, Tanah Merah, Kelantan; and logging sites in Tasek Kenyir, Hulu Terengganu. Notes: Average rainfall recorded in the current study was between 125.6–414.9 mm (Malaysian Meteorology Department, 2016, 2017); SE: Standard error; Δ: Elevations (m a.s.l.) above sea level; ARH (1–100%): Air Relative Humidity; SM (1–10%): Soil Moisture; LI (lx): Light Intensity in Lux unit; Min: Minimum value; Max: Maximum value; N-value (Logging Sites) = 15; N-value (DSFs) = 6. Different superscripts indicate significant differences (p<0.05) in Kruskal-Wallis one-way ANOVA with multiple pairwise comparisons.

ARH SM Disturbed Forests Temperature (oC) LI (lx) Δ (1–100%) (1–10%)

a a a a Disturbed Secondary Min: 28.8±0.5 Min: 75.8±1.6 Min: 3856.7±1193.0 Min: 2.2±0.3 44.4-129.9 Forests (DSFs) Max: 31.1±0.3b Max: 88.0±2.4c Max: 17833.3±1641.5c Max: 3.3±0.5b

Min: 31.2±1.1a Min: 67.0±2.3b Min: 9180.0±1177.7b Min: 2.0±0.4a Logging Sites (logged 98.8-244.6 forests) Max: 34.9±1.0c Max: 86.7±1.7c Max: 17866.7±960.5c Max: 3.2±0.9b

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Figure 2. In-situ ecology parameters recorded in disturbed forests of Terengganu and Kelantan regions. A. Mean values of Minimum Temperature. B. Mean values of Maximum Temperature. C. Mean values of Minimum ARH. D. Mean values of Maximum ARH. E. Mean values of Minimum Light Intensity. F. Mean values of Maximum Light Intensity. G. Mean values of Minimum Soil Moisture. H. Mean values of Maximum Soil Moisture. Mean±SE is the means with standard error of the each parameter. Different superscripts indicate significant differences (p<0.05) in Kruskal-Wallis one-way ANOVA with multiple pairwise comparisons.

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Discussion the atmospheric and soil microclimatic stratifications Relationship between species abundance, species (Werner & Gradstein 2009, Benίtez et al. 2015), thus density and the habitat type.– The abundance of killing all the exposed epiphytic and terrestrial plants. orchids and their survival in the disturbed forests were Small changes in ecological conditions may be driven by the intensity of disturbance faced by each deleterious to intolerant species. Even slight differences population in their particular habitat. The results show in the humidity may be significant for species near that the mildly disturbed secondary forests had a higher their threshold levels of water supply (Werner & orchid density than the highly disturbed logging sites. Gradstein 2009), especially epiphytes. Orchids are This was certainly due to the ecosystem variations resistant and adaptive towards distress environmental altered by the anthropogenic-driven disturbances. conditions as long as atmospheric and soil moisture These variations were linked to the weather and levels and sunlight intensity are tolerable for their microclimatic conditions, especially temperature, survival (Hietz et al. 2006). Nevertheless, they would humidity, precipitation, and light intensity, and also flourish better in less disturbed areas under the forest the presence of supporting trees and organisms such as canopy where they can obtain optimal light, water, and fungi, mosses, and pollinators. nutrients to reach maturity for reproduction (López & In comparison, the secondary forests clearly had Runkle 2005). Therefore, it is highly recommended a healthier environment for orchid survival as the that the secondary forest and forest fragments left after habitat conditions (moisture and nutrient availabilities) logging are identified and protected as these areas were were still suitable for the growth of both epiphytic observed to still harbour precious orchid species. and terrestrial orchids. Furthermore, the presence of standing and healthy trees gave a better support for the Study based on subfamilies and growth habits.– epiphytic orchids. The trees were significant in assisting Subfamily Epidendroideae was found to be the best orchid photosynthesis, and also the pollination and represented in our study areas. They are predominantly reproduction (Cribb et al. 2003, Cozzolino & Widmer epiphytic and often have aerial roots (Holttum 1964, 2005). Seidenfaden & Wood 1992). In the current study, Studies have shown that terrestrial orchids do not only one species of this subfamily, Calanthe ceciliae, survive in secondary habitats or invaded conserved was found growing as a terrestrial in the logging forest (Williams-Linera et al. 1995, Bergman et sites. Compared to the other lineages, orchids from al. 2006). However, several small populations of this subfamily are known to have a wide distribution terrestrial Apostasia nuda R.Br. and Corymborkis area along the elevation gradients. They are always veratrifolia were found in the DSFs of Kuala Koh found to be abundant in extreme environments, and Tanah Merah. Despite of the heavily damaged by are disturbance-resilient and exhibit more drought- mudslides and heavy flooding since 2014, there are tolerance characteristics when compared with the some pockets of the forests that were not affected and other subfamilies (Rada & Jaimez 1992, Zhang et al. terrestrial orchids are still found there. The fragments 2015, Yang et al. 2016). Previous studies of degraded of the unlogged forests are still very much protected vegetation indicated the success of vascular epiphytes, by the forest canopy from the sun, and thus provide a including epiphytic orchids entirely belonging to tolerable environment for the orchid growth. This is Epidendroideae subfamily (Hietz et al. 2006, Werner where small populations of the terrestrials Calanthe & Gradstein 2009, Huda & Wilcock 2011). This ceciliae Rchb.f. and Hetaeria oblongifolia Blume subfamily is largely characterized as shade-loving were found. The low number of terrestrial orchids species and only a small number are sun-loving. It in the logged forests was greatly attributed to the might be expected that shade-demanding species poor soil condition, where humus-rich soil surface would find habitat in open forests with direct exposure was eroded badly during logging that alters the pH, to the sun’s rays, such as logging sites, less favourable. humidity and the nutrients. The full exposure to Although, conversely, sun-loving epiphytic orchids, sunlight and the radiation heats up the surface in the such as Bromheadia Lindl. with tough stem and logged forest without canopy protection had distorted many small or terete leaves, should find the high light

LANKESTERIANA 19(2). 2019. © Universidad de Costa Rica, 2019. 118 LANKESTERIANA environment in the opened forest equally represented strategies. According to local villagers, the logging in the upper canopy of the closed forest (Hietz et al. activity in Petuang had started some years (unspecified) 2006). before the logging activity in Gawi that began in 2014. None species of Cypripedioideae and Vanilloideae Thus, time wise, it implies that the orchids in Petuang subfamilies were recorded from the studied sites. had been exposed longer to the extreme environment Cypripedioideae is mostly terrestrial, with a few conditions, plus, a high number of them were found epiphytes and lithophytes; in our area, species degraded with severe sun-damage and dehydration belonging to this subfamily are highland species with during the field collections, when compared with our coriaceous or leathery leaves, without pseudobulbs and collections from Gawi. only adapted to wet and cool conditions (Seidenfaden The epiphytic orchids have advanced adaptations & Wood 1992). Meanwhile, Vanilloideae has both of one or more organs to allow them to survive the long warm and cool growing species, yet, have always had warm and dry environment conditions. Bulbophyllum been recorded with lower occurrence in Peninsular and Dendrobium species for example have storage Malaysia, except for Vanilla griffithii Rchb.f., a organs like pseudobulbs and pseudobulbous stems, commonly found species in lowland and swamp fleshy or leathery leaves, and aerial roots with velamen forests (Go & Hamzah 2008, Go et al. 2011). as a protective layer against water loss (Zotz & Winkler 2013, Zhang et al. 2015) and sun radiation damage Dominance of epiphytic orchids in logging sites.– (Chomicki et al. 2015), including Thrixspermum Epiphyte diversity tends to be reduced markedly Lour, and the leafless orchids Taeniophyllum Blume following disturbance (Wolf 2005, Nöske et al. 2008), that have photosynthetic roots. Unfortunately, having with variation due to the severity of disturbance and adaptations that allow them to survive the long the types of disturbed habitat studied (Hietz 2005, warm and dry conditions do not help them to survive Holz & Gradstein 2005). Conversely, in the current extended periods of desiccation since most of the study, there was a high abundance of epiphytic orchids specimens collected in this study exhibited dormancy found in the logging sites (Fig. 3). and were dying upon collection. However, this does not suggest that orchid diversity and abundance increases with the intensity of Effects of anthropogenic-driven disturbances towards anthropogenic-driven disturbance. A high abundance orchids abundance and survival in the disturbed of epiphytic orchids and the significant difference forests.– The relationship between environmental in densities of orchids recorded between the logging conditions and orchid abundance has been frequently sites in Tasek Kenyir area are assumed to be correlated reported, but little is understood for orchid responses with the abundance or densities of the fallen trees towards micro-climatic challenges and their abundance in the logging sites, disturbance-induced dryness in the degraded forest with extremely fragmented stresses, durations of exposure to the anthropogenic- tree canopies and vegetation. The canopy disruptions induced disturbance (claim is made based on a survey caused by clear-cut logging produced openings in and empirical evidence), and less favourable soil the canopy, which had significantly affect ambient conditions for the terrestrial orchids to flourish at both temperature and moisture. In the undisturbed-closed sites studied. forest, the sun irradiation is converted into heat at the A further study on the effect of human-induced interface of the atmosphere and canopy (Werner & environmental disturbance on the survival of orchid Gradstein 2009). The heat intensity was more severe community in the degraded forests would help in disturbed-opened canopy forests or clear felling government agencies, conservation biologists and logging sites. policy makers in formulating better conservation The microclimate of the disturbed forests

Right, Figure 3. Epiphytic orchids on the fallen trees and ground threatened by direct exposure to the sun irradiation and dryness in the logging sites of Tasek Kenyir area. A. Callostylis pulchella, Renanthera histrionica, Pinalia maingayi. B. Cleisostoma scortechinii. C. Coelogyne cumingii. D, E. Grammatophyllum speciosum. F, G, H. Coelogyne foerstermannii. Photos by DigitalDome.

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LANKESTERIANA 19(2). 2019. © Universidad de Costa Rica, 2019. 120 LANKESTERIANA showed lower ARH and extremely high surrounding possibilities: (i) reduction of the chlorophyll content temperature if compared to undisturbed forested area. which has reduced the pigment responsible for the The direct exposure to sun radiation and heat had green colour of the leaves; (ii) too high light intensity imposed desiccation, a state of extreme dryness, and provokes an increase in leaf temperature causing drought-heat physiological stress towards the exposed photosynthetic machinery degradation in plant cells orchid community in the forest. Deriving from a study (Edmond et al. 1978, Sinha & Häder 2002, Stancato et tested on an epiphytic orchid leaves, Phalaenopsis, al. 2002, Chomicki et al. 2015). the optimal temperature for photosynthetic carbon The deviations occurred to the data collected in fixation ranges from 29/25 ºC to 32/28 ºC day/night the current study for light intensities could be related temperature (Guo & Lee 2006, Guo et al. 2012). But, to various reasons, including time of the day, season, the temperature recorded for the logging sites in the geographic location, weather, or device systematic current study was much higher and exceeded the error. The light intensity could be also affected by optimal range required for energy production through dust particles and atmospheric water vapor, slope photosynthesis. The heat irradiation caused burn and and elevation (Edmond et al. 1978). The units Lux is browning of the plant parts, which would eventually simply based on visual sensitivity and do not provide lead to injuries and death. information on the energy or photon content of light, Generally, the higher the temperature, the lower which truly influences the photosynthesis or sugar the humidity or moisture, and biologically, it means the production in the leaf. Hence, in order to understand lower the turgor pressure in plant cells. The changes better the light intensity for a study relating to plant in turgor pressure in cells and tissues could also responses, the suitable unit is the μmol m-2s-1 trigger the signal transduction pathways (Beauzamy [number of photons received per unit time (s) on a unit et al. 2014) and structural proteins (Yooyongwech area (m)]. Similarly, the effects of ultraviolet radiation et al. 2008) involved in flower development: flower (UV-radiation) on orchids in wide-opened canopy opening, anther dehiscence, and pollen tube growth. forest are another perspective recommended for future Thus, the exhibitions of signs of dying such as flowers studies of orchids in disturbed forest. UV-radiation is a or buds browning, flowers or buds dropping off (bud or major hazard for living organisms exposed to sunlight, bloom blast) and dormant, and pseudobulbs browning causing DNA mutation, and plasma membrane lipid and shriveled in the disturbed forests during the field peroxidation. collections were most caused by high temperature A small number of terrestrial orchids encountered (extreme heat irradiation) and extreme dryness during in this study were suspected to be influenced by the drought season. soil properties and ground conditions. Inconclusively, Moreover, the bloom and bud blast are generally aside from the massive clearance of ground vegetation orchid’s reactions to environmental shock and is by tractor, the low values of soil moisture (SM) and the plant’s way of protecting itself. This might be absence of buffering trees and leaf litter were predicted brought on by a sudden change in temperature and to reflect and influence the geographical distribution of reduced water potential in plant cells to trigger the the individual terrestrial orchids in the logged forests flower or bud development. By shedding its buds, the and DSFs. Soil moisture was included as the predictor, orchid can divert more energy to maintaining its vital because, even though moisture affected by soil- systems (Beauzamy et al. 2014). A continuous sugar or forming factors (mineralization and holding capacity), carbohydrate supply to the apex of a reproductive bud moisture potentially is a strong factor controls other through photosynthetic carbon fixation is essential for soil properties, including pH and nutrient (Pulla et continued floral development (Wang 1995, Konow & al. 2016). Although, the min and max values of SM Wang 2001). Therefore, maximizing sugar production recorded for both sites were not statistically significant with optimal light intensity is important for orchid different, nonetheless, in comparison, it appears that growth and flowering (Guo et al. 2012). the min moisture values recorded for logging sites were The browning observed on the leaves of orchids lower than the moisture values recorded in a previous collected from the logging sites could be due to two study on soil properties associated with dry forest

LANKESTERIANA 19(2). 2019. © Universidad de Costa Rica, 2019. Besi et al. — Orchid diversity in anthropogenic-induced degraded tropical rainforest 121 community (see Pulla et al. 2016). This suggests that 3 years’ botanical collections. We anticipate much the dryness stress faced by the orchids community in more orchids at risk could be found in the logged forest the logging sites was much severe than in the naturally following the positive correlation between the density occurred dry forest. of epiphytic orchids and the density of fallen trees in The surface erosion occurred in the logging sites as the logging sites. This orchid community appears to be a result of absence of buffering trees and leaf litter, and critically endangered due to ongoing logging activities direct exposure of mineral soil to the impact of rain in the region. The canopy disruptions caused by forest might have reduced the soil holding capacity which logging and the mudslides had reduced the quality of the would have also reduced the soil moisture and nutrient orchid habitats. The anthropogenic-driven disturbances (Raghubanshi 1992, Li et al. 2014), and compromising had harmfully altered the humidity and temperature in the orchid growth and their mycorrhizal association the affected areas. The disturbance-induced drought (Batty et al. 2001, Harrington & Schoenholtz 2010, stress had damaged the orchid morphologically and Li et al. 2014). Increased frequency of erosions and interfered with their phenology. This study has resulted direct heat exposure would affect the microorganism in new hope for rapid orchid species documentation community, too. In nature, primarily, the terrestrial endeavour in Malaysia, as many epiphytic orchids are orchids also require the mycorrhizal association accessible resulting in many new discoveries of new (fungal-roots) for survival and nitrogen fixation records and species to science. (Brundrett 2002). For a better understanding, it is desirable to include soil pH in future studies for a better clarification and to determine the relationship between level of mineralization and nitrification of soil Acknowledgements. We would like to extend our and orchid distribution in the disturbed forest. appreciation to the Forest Department Peninsular Malaysia and Department of Wildlife and National Conclusions. Our results show a high diversity of Parks Peninsular Malaysia for granting us the permit [Reference No. JH/100 Jld. 16(14)] to access the studied orchids found at Peninsular Malaysia’s disturbed forest areas and to the UPM-KRIBB (Korea Research Institute areas. The diversity indexes reflect a greater orchid of Bioscience and Biotechnology) Vot. 6384300, and diversity in the areas with wide-opened canopies of the Universiti Putra Malaysia for the research funding (Putra logged forests than in the canopy-covered DSFs, with Grant No. 9413603), and Yayasan Biasiswa Tunku Abdul several rare species and six species being endemic Rahman (YBSTAR) scheme for sponsoring this Master to Peninsular Malaysia, including two new species of Science degree undertaking. The authors are also very to science, and of these, largely were epiphytes, thankful to the staff and friends in the department for typically with robust morphological appearance and their support and invaluable assistance throughout this project. We owe our sincere thanks to many experts adaptations. This high species diversity and indexes for their opinions and helps on the identifications; in wide-opened canopies logged forests is due to Jeffrey Champion (Bedugul Tabanan, Bali, ), accessibility of epiphytic orchids on fallen trees. The Jim Cootes (Centre for Plant Biodiversity Research, current study covered only 5% of the total area of the Canberra, ), and Linus Gokusing (Kipandi disturbed forests in Terengganu and Kelantan through Park, Malaysia).

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